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Journal of Emerging Diseases and Virology
ISSN 2473-1846
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Mini Review
Open Access
Volume: 3.1
Avian Influenza Infections in Humans and Poultry
of Lebanon: A Mini Review
Muhammad Murtada1, Elie Barbour1,2 and Houssam Shaib1,*
Faculty of Agricultural and Food Sciences, Department of Agriculture, American University of Beirut,
Lebanon
2
Adjunct to Biochemistry Department, Faculty of Science, and Production of Bioproducts for Industrial
Applications Research Group, King Abdulaziz University, Jeddah, Saudi Arabia
1
Corresponding author: Houssam Shaib, Faculty of Agricultural and Food Sciences,
American University of Beirut, Beirut, Lebanon; Tel: 009613504316; Fax: 009611744460;
E-mail: [email protected]
*
Received date: 07 Nov 2016; Accepted date: 09
Dec 2016; Published date: 15 Dec 2016.
Citation: Murtada M, Barbour E, Shaib H (2016)
Avian Influenza Infections in Humans and Poultry of
Lebanon: A Mini Review. J Emerg Dis Virol 3(1): doi
http://dx.doi.org/10.16966/2473-1846.125
Copyright: © 2016 Murtada M, et al. This is an
open-access article distributed under the terms
of the Creative Commons Attribution License,
which permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Abstract
Avian Influenza (AI), commonly known as “bird flu” is a viral disease that affects birds with usually asymptomatic signs in wild birds and
waterfowls. In poultry, avian influenza causes high economic losses and was previously referred to as “fowl plague” in the first reported outbreak
in 1878 in Italy. AI is usually host specific affecting mostly gallinaceous species. However, interspecies transmission from birds to humans was first
documented in 1997 in Hong Kong leading to 18 human infections with highly pathogenic avian influenza (HPAI) H5N1 and 6 deaths caused by
human exposure to poultry in live bird markets. Since then, not only HPAI H5N1 became of major public health significance causing most of the
reported AI human illnesses and deaths, but also low pathogenic H5N1 and other subtypes, including H9N2 and H7 that are highly mutagenic and
can convert into HPAI strains in a relatively short period of time.
Lebanon is a Mediterranean country located between major migratory bird flyways with a large population of domestic and wild bird species.
Consequently, repeated AI outbreaks in poultry were recorded and documented in this country as the outbreak of 2006. This paper reviews
previous reports on LPAI in poultry (H9 and H7) and humans (H9, H4 and H11) and includes the first HPAI H5N1 outbreak in domestic poultry. The
potential of local AI viruses to evolve into highly pathogenic and/or zoonotic is discussed. Prevention and preparedness practices to confront the
AI issue, using One Health approach is addressed.
Keywords: Avian influenza; Pathogenicity; Zoonosis
AI in Poultry
Avian influenza disease that affects bird species is caused by viruses
belonging to the family Orthomyxoviridae and genus Influenza virus A [1].
Avian influenza A viruses are known to be host specific infecting mainly
wild and domestic bird species. In addition, HPAI H5N1 infections were
reported in the early 2000s in leopards, tigers, domestic cats, dogs, stone
martins, civets, and domestic pigs that were exposed to infected birds,
without becoming endemic in these species [2-6]. Influenza A viruses
has antigenically related matrix and nucleocapsid proteins, however
are subtyped based on their hemagglutinin (H) and neuraminidase (N)
proteins. Eighteen haemagglutinin (H1-H18) and 11 neuraminidase
(N1-N9) have been recognized [7]. Each type is recognized by its own
combination of one H and one N antigen [1]. Avian Influenza viruses
are divided into two groups according to the virulence of the strain and
its ability to cause high mortality in poultry. The first group is highly
pathogenic avian influenza (HPAI) that is known to cause flock mortality
of up to 100% [1]. H5, H7 and H9 are the only subtypes causing HPAI to
date [8]. Nonetheless, not all of these subtypes cause HPAI; many cause
milder disease in poultry and are grouped under Low Pathogenic Avian
Influenza (LPAI). HPAI and LPAI H5/H7 that might become highly
pathogenic by mutation are both on the OIE list of notifiable diseases [8].
AI was first reported as “Fowl Plague” referring to highly pathogenic avian
influenza (HPAI) in 1878 by Perroncito in Italy [9].Economic losses from
AI are mainly caused by HPAI that causes severe mortality in domestic
birds. Additional inputs result from HPAI outbreaks, including the cost of:
disposal, depopulation, cleaning, disinfection, quarantine, and surveillance
cost, and losses from high mortality and morbidity and indemnities paid
for birds [10]. However, indirect costs such as losses in poultry exports,
farmer’s loss of income, and decrease in consumer demand for poultry
can increase losses by 5-10 folds. For instance, significant economic losses
were caused by HPAI outbreaks in United States from December 2015
through July 2015. During these outbreaks 48 billion birds mostly laying
hens (38.4 million) were depopulated at an estimated direct cost of $1.6
billion with economy-wide impact estimated at $3.3 billion [11]. Losses
from LPAI are mostly due to a secondary infection in birds and include
mortality, carcass condemnations, secondary bacterial medications,
cleaning and disinfection and delayed placement of new flocks [10]. LPAI
endemics such as H9N2 poultry infection in Asia and the Middle East in
the late 1990s and early 2000s, and H5N2 in Mexico, in the 1990s, have
caused great economic losses that were poorly reported [10].
AI in Lebanon
Lebanon is a Mediterranean country located in the Middle East,
Asia, surrounded by countries that have reported poultry and human
infection with HPAI H5. Moreover, Lebanon lies between 2 important
wild bird migratory flyways, the Black Sea/Mediterranean flyway and the
East Africa/West Asia flyway [12].Lebanon has a high domestic poultry
population of about 80.8 million birds divided into 77 million broilers and
3.8 million laying hens [13]. Lebanon also neighbors Syria and currently
witnesses increased illegal movement of domestic animals from Syria to
Lebanon due to the current War situation in Syria and the uncontrolled
boundaries. All of these facts increase the risks of AI spread in Lebanese
poultry and human populations.
LPAI in Lebanese poultry
Low pathogenic avian influenza (LPAI) in Lebanon was first reported
as H9N2 in 2006 by Barbour et al [14]. This outbreak caused significant
decrease in egg production of 46% in broiler breeder and 47.3% in laying
Copyright: © 2016 Murtada M, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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hen farms. Flocks were confirmed for AI using ELISA and then random
ELISA-positive samples revealed H9 specific antibodies by HI test. The
virus was further subtyped as H9N2 by Central Veterinary Laboratory in
Weybridge, UK. Reporting of H9N2 was not limited to poultry; specific
H9 antibodies were also found in pigs eating infected poultry at 100%
[14]. The second infection of Influenza type A was reportedby the same
researcher in 2007. In a collaborative work between the Lebanese Ministry
of Agriculture and the American University of Beirut, a surveillance of
type A influenza viruses was conducted in migratory wild birds, resident
wild birds, pet birds and farm birds, using the reverse transcriptionpolymerase chain reaction (RT-PCR) technique. Results showed that
14.3% of the collected samples were positive for AI. All positive samples
underwent RT-PCR subtyping for H5 and H7 genes and were negative for
H5. Only 6.8% of the AI positive samples were found to be of the LPAI H7
type. The H7 positive samples were restricted only to sparrows (resident
wild bird species) and to backyard chicken in the southprovenance of
Lebanon [15].
Pathogenicity and oseltamivir resistance of LPAI isolated from
broilers in Lebanon
Although losses from LPAI viruses are lower, compared to those
resulting from HPAI; H9N2 LPAI viruses in Lebanon demonstrated an
ability to increase their pathogenicity, and host range, following their
passaging in different hosts. A study was conducted to evaluate the effect
of nasal viral passaging of Lebanese isolate of H9N2 AI virus in hamsters
on its interspecies-pathogenic adaptability by monitoring the variation in
amino acid sequences of hemagglutinin (HA) and neuraminidase (NA)
proteins [16]. Results showed that there was 100% similarity in amino acid
sequence of HA gene in most passaged viruses. The amino acid sequence
of the neuraminidase gene showed an antigenic drift caused by a R46P
point mutation that might explain the pathogenic adaptability of the third
passage viruses in hamsters’ lungs [16]. The isolated R46P H9N2 virus
showed resistance to oseltamivir in comparison with other three H9N2
viruses that were susceptible at a percentage ranging between 63-100%
[17].These results confirm the World Health Organization’s alertness for
possible zoonotic potential of adaptable H9N2 [16]. Another similar study
was done on broilers by multiple passages of H9N2. This work resulted in
conserved dibasic R-S-S-R amino acid sequence of the viral hemagglutinin
cleavage site and a variability in the neuraminidase amino acid sequence.
These changes were also associated with higher pathogenicity in the third
and final passage H9N2 viruses that was apparent by increased morbidity
[18]. A third study of multiple passages of LPAI H9N2 was conducted in
chicken embryos. The mortality among chicken embryos jumped from
0% in passage 0 original H9N2 virus to 86.7% and 100% of second and
third H9N2 passages respectively [19]. Results indicate that antigenic drift
caused by point mutations of the neuraminidase viral proteins occur under
selective pressure of immune responses. These point mutations prove that
in addition to antigenic shifts caused by viral reassortment, antigenic
drifts can play a role in the increased pathogenicity and persistence of
LPAI viruses in population [20].
HPAI H5N1 in Lebanon
Recently, on the 23rd of April 2016 Lebanon officially reported, for the
first time, HPAI in domestic poultry farm in the village of Nabichit in
Bekaa region located near the Lebanese-Syrian border [21]. The owner
of the farm reported abnormal flock mortality reaching up to 100%. The
infected chicken farm and other surrounding farms were immediately
zoned and put under quarantine. Twenty thousand birds were dead due
to HPAI infection and 60000 were stamped out [21]. Three weeks later,
the second outbreak of HPAI H5N1 was reported to the OIE on 14th
of June 2016 in a nearby chicken layers farm located in Sariin Tehta in
the protection zone around the primary reported outbreak [22]. In the
second outbreak 20000 birds died from HPAI infection and 106000 birds
Open Access
in nearby farms were stamped out. The source of the two outbreaks was
reported to be illegal animal movement from Syria to Lebanon [21,22] that
is currently increasing due to the war situation in Syria and uncontrolled
boundaries between the two countries. HPAI H5N1 outbreaks in Lebanon
caused a great public health concern about the possibility of HPAI
transmission to humans through the consumption of poultry eggs and
meat.Consequently, chicken live weight prices and prices of eggs reached
the lowest recorded decrease in 2016 reflecting the economic impact of
H5N1 on the poultry sector.
AI in Humans
Interspecies transmission of type A AI from birds to humans was firstly
documented in 1997 in Hong Kong leading to 18 human infections with
highly pathogenic avian influenza (HPAI) H5N1 and 6 deaths caused by
human exposure to birds [23].
Since then, HPAI H5N1 and LPAI H7N9 were proved to be of greatest
zoonotic potential becoming a major public health concern and causing
most of the reported AI human illnesses and deaths [24]. Exposure to live
birds has been a major risk factor associated with most of the AI human cases.
Factors restricting the host range of avian influenza A Viruses
Influenza viruses belonging to the Orthomyxoviridae family are divided
into A, B and C based on group specific antigens. Only influenza type
A viruses that include avian and swine influenza viruses are of zoonotic
importance [25]. AI viruses are known to infect mostly avian species and
rarely humans unlike the human H1N1 and H3N2 influenzas that occur
each year [26]. Differences in influenza transmission and replication
may arise from the variation in cell receptor specificity in the respiratory
tract epithelium of the host. Avian influenza viruses bind preferably to
N-acetylneuraminic acid-α2,3-galactose linkage on sial-oligosaccharide
(α2,3 linkage) receptors, while human influenza viruses bind preferably to
N-acetylneuraminic acid-α2,6-galactose linkage on sial-oligosaccharide
(α2,6 linkage) receptors. Avian respiratory epithelium has predominant
α2,3 linkage but human respiratory epithelium has predominant α2,6
linkage. Although the human respiratory tract does have α2,3 receptors in
cells deep in the respiratory system, the location of these receptors make
human AI viral infections infrequent [27]. Moreover, the AI polymerase
complex and other viral genes may be also responsible for inefficient
replication in humans [27].
The second factor that plays an important role in restricting the host
range of AI is the proteolysis of the hemagglutinin that is done by cellular
proteases in the HA cleavage site to make the virus infectious. Mammalian
influenza viruses have arginine amino acid that marks the HA cleavage
site. Proteases able to split this site are only found in epithelial cells of
mammalian respiratory system making mammalian influenza infection
restricted to the respiratory system [20]. However, avian influenza viruses
have multi-basis amino acids on the cleavage site making AI infection
in birds a systemic infection since all body organs of birds contain the
ubiquitous proteases that are able to bind and split the cleavage site. Moreover,
bacterial proteases from Staphylococcus aureus, Streptococcus pneumonia,
Haemophilus influenza, or Klebsiella spp., are able to split the HA cleavage
site and activate the virus causing human infection with AI [28].
Avian influenza virus infection in humans
H5N1 was the first avian influenza virus reported to infect humans in
1997. A global epidemiological study showed that there were 907 H5N1
human cases between May 1997 and April 2015 of whom 483 case fatalities
occurred 53.5% yielding H5N1 to impose the highest zoonotic threat
[29].The second type of AI viruses isolated from humans was H9N2 [30].
Both H5 and H9 AI viruses were genetically linked to AI found in quails
[20]. More subtypes of AI in humans were isolated from humans, namely
Citation: Murtada M, Barbour E, Shaib H (2016) Avian Influenza Infections in Humans and Poultry of Lebanon: A Mini Review. J Emerg Dis Virol 3(1): doi
http://dx.doi.org/10.16966/2473-1846.125
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Open Access
H7N7 and H7N9 [31,32]. Avian influenza subtype H7N7 was isolated in
an epizootic in the Netherlands in 2003. Several people were infected and
one case fatality was reported during the 2003 H7N7 outbreak [31]. In
2013, a new AI subtype, namely H7N9 virus was isolated from human
patients in China. The H7N9 LPAI caused 440 human infections with
at least 155 deaths from the disease showing symptoms of high fever,
bronchitis, pneumonia, and dyspnea [32].
LPAI human infections and the risk of HPAI H5N1 human
infection in Lebanon
In Lebanon, reported AI human infections belong to LPAI group.
Lebanese scholars found that 32.3% of individuals exposed to H9 infected
poultry had elevated antibody titer again viruses of the same subtypes
[14]. Using serological tests, Kayali et al. [12] showed a cross-sectional
evidence of human infection with H4 and H11 avian influenza viruses
among Lebanese chicken growers. Although no symptoms have been
observed among farmers, this study indicated that H4 and H11 LPAI
can be of zoonotic importance. Moreover, human exposure to live
birds was still recognized as a major risk factor in AI human infections.
Although, recently, Lebanon reported HPAI in domestic poultry [21,22],
human infection with HPAI is still not evident in this country. Epizootic
HPAI H5N1 in Lebanon caused a great public health concern about the
possibility of HPAI transmission to humans through the consumption of
poultry eggs and meat. Literature review shows that AI human infections
were mostly restricted to exposure to live poultry and not to consumption
of poultry products, with no evidence of human-to-human transmission
[33]. In Lebanon feeding dead birds to swine is a common practice [15].
This fact adds up to the risk of human infection with HPAI since pigs might
act as a reassortment vessel when infected with both human and avian
influenza viruses rendering HPAI adaptable for human transmission.
A recent research reported that humans could also be a “mixing vessel”
when dually infected with human and avian influenza viruses at the same
time [34]. This means that poultry farmers and workers in Lebanon are
at a high risk of human H5N1 infections after the first reported HPAI
H5N1 in poultry. Table 1 summarizes the confirmed human and poultry
infection with AI viruses in Lebanon from 2006 to present.
due to the fact that these viruses can mutate into HPAI type, widen their
host range, besides their resistance characteristics to anti-influenza drugs,
namely oseltamivir.
The Government of Lebanon should conduct continuous surveillance
and not only sporadic targeted surveillance to monitor HPAI in poultry,
high risk individuals exposed to poultry and wild birds. Moreover, the
Government of Lebanon should appoint a team having One Health
Approach to tackle this risk and put a preparedness plan for any future
human infection with H5N1 in Lebanon. Research should backup
governmental efforts in controlling AI outbreaks, specifically in developing
innovative vaccines for poultry.
References
1.
Capua I, Alexander DJ (2009) Avian influenza infection in birds: a
challenge and opportunity for the poultry veterinarian. Poult Sci 88:
842-846.
2.
Choi YK, Nguyen TD, Ozaki H, Webby RJ, Puthavathana P, et al.
(2005) Studies of H5N1 influenza virus infection of pigs by using
viruses isolated in Vietnam and Thailand in 2004. J Virol 79: 1082110825.
3.
Keawcharoen J, Oraveerakul K, Kuiken T, Fouchier RA, Amonsin A, et
al. (2004) Avian influenza H5N1 in tigers and leopards. Emerg Infect
Dis 10: 2189-2191.
4.
Kuiken T, Rimmelzwaan G, van Riel D, van Amerongen G, Baars M, et
al. (2004) Avian H5N1 influenza in cats. Science 306: 241-241.
5.
Roberton SI, Bell DJ, Smith GJD, Nicholls JM, Chan KH, et al. (2006)
Avian influenza H5N1 in viverrids: implications for wildlife health and
conservation. Proc Biol Sci 273: 1729-1732.
6.
Songserm T, Amonsin A, Jam-on R, Sae-Heng N, Pariyothorn N, et
al. (2006) Fatal avian influenza A H5N1 in a dog. Emerg Infect Dis 12:
1744-1747.
7.
Tong X, Zhu X, Li Y, Shi M, Zhang J, et al. (2013) New World Bats
Harbor Diverse Influenza A Viruses. PLoS Pathog 9: e1003657.
8.
OIE (2-15) OIE Terrestrial Manual 2015. Avian influenza (infection with
avian influenza viruses). May 2015.
Conclusion and Recommendation
9.
Both types of avian influenza viruses (LPAI and HPAI) are circulating
in Lebanon. Low Pathogenic avian influenza viruses were detected in both
poultry and farmers. So far, highly pathogenic avian influenza viruses
were only reported in poultry. Regarding HPAI, Lebanon might witness
sporadic outbreaks in poultry leading to economic losses and public
health concerns. In addition, Lebanese LPAI viruses pose serious threat
Stubbs EL (1948) Fowl Pest. In: Biester HE and Schwarte LH.
Diseases of Poultry. 2nd Edition, Ames, Iowa. Iowa State University
Press.
10. Swayne DE, Halvorson DA (2008) Influenza. In: Fadly AM, Glisson
JR, McDougald LR, Nolan LK, Swayne DE. Diseases of poultry. 12th
Edition. Blackwell Publishing Ltd. Ames, Iowa. 153-189.
Year
Subtype
2006
2006
2006
2007
2007
2007
2007
2007
2007
2010
2010
2016
2016
H9N2
H9N2
H9N2
AI type/ not typed
AI type/ not typed
AI type/ not typed
AI type/ not typed
H7
H7
H4
H11
H5N1
H5N1
Patho
type
LPAI
LPAI
LPAI
LPAI
LPAI
LPAI
LPAI
LPAI
LPAI
LPAI
LPAI
HPAI
HPAI
Host species
Affected Reference
Humans
11
Pigs
3
Domestic Poultry
24 farms
Domestic Poultry
134
Pet Birds
11
Resident Wild Birds
15
Migratory Birds
30
Domestic Poultry
12
Resident Wild Birds
1
Humans
3
Humans
2
Domestic Poultry
20000
Domestic Poultry
20000
[14]
[14]
[14]
[15]
[15]
[15]
[15]
[15]
[15]
[12]
[12]
[21]
[22]
Table 1: List of confirmed human and poultry infections with avian influenza
viruses in Lebanon from 2006 to present
11. Greene JL (2015) Update on the Highly-Pathogenic Avian Influenza
Outbreak of 2014-2015. Cong Res Serv 1-18.
12. Kayali G, Barbour E, Dbaibo G, Tabet C, Saade M, et al. (2011)
Evidence of infection with H4 and H11 avian influenza viruses among
Lebanese chicken growers. PLoS One 6: e26818.
13. FAOSTAT (2016).
14. Barbour EK, Sagherian VK, Sagherian NK, Dankar SK, Jaber LS,
et al. (2006) Avian influenza outbreak in poultry in the Lebanon and
transmission to neighbouring farmers and swine. Vet Ital 42: 77-85.
15. Barbour EK, Shaib HA, Rayya EG (2007) Reverse transcriptasepolymerase chain reaction-based surveillance of type A influenza
viruses in wild and domestic birds of the Lebanon. Vet Ital 43: 33-41.
16. Shaib HA, Cochet N, Ribeiro T, Nour AMA, Nemer G, et al. (2014)
Passaging impact of H9N2 avian influenza virus in hamsters on its
pathogenicity and genetic variability. J Infect Dev Ctries 8: 570-580.
17. Kumosani T, Ahmadieh DM, Shaib HA, Hamadeh SK, Jaber LS, et al.
(2015) Oseltamivir activity against avian influenza H9N2 strain with
different point mutations in their neuraminidase. Vet Ital 51: 217-224.
Citation: Murtada M, Barbour E, Shaib H (2016) Avian Influenza Infections in Humans and Poultry of Lebanon: A Mini Review. J Emerg Dis Virol 3(1): doi
http://dx.doi.org/10.16966/2473-1846.125
3
Sci Forschen
Open HUB for Scientific Researc h
18. Shaib HA, Cochet N, Ribeiro T, Nour AMA, Nemer G, et al. (2011)
Pathogenicity and amino acid sequences of hemagglutinin cleavage
site and neuraminidase stalk of differently passaged H9N2-avian
influenza virus in broilers. Adv Bio sci Biotech, 2011.
19. Shaib H A, Cochet N, Ribeiro T, Nour AMA, Nemer G, at al. (2010)
Impact of embryonic passaging of H9N2 virus on pathogenicity and
stability of HA1-amino acid sequence cleavage site. Med Sci Monit
16: BR333-BR337.
20. Bauerfeind R, Liebig J, Von Graevenitz A, Kimmig P, Schwarz TF et
al. (2015) Zoonoses: Infectious Diseases Transmissible from Animals
to Humans. 4th ed. ASM Press.
21. OIE (2016) Highly Pathogenic Avian Influenza Outbreak in Lebanon.
Immediate notification.
22. OIE (2016) Highly Pathogenic Avian influenza Outbreak in Lebanon.
Follow-up report No. 1 (Final report).
23. Chan P K (2002) Outbreak of avian influenza A (H5N1) virus infection
in Hong Kong in 1997. Clin Infect Dis 34: S58-S64.
24. CDC (2016) Avian Influenza A virus infection in humans.
25. Van Reeth K (2007) Avian and swine influenza viruses: our current
understanding of the zoonotic risk. Vet Res, 38: 243-260.
26. Ito T, Couceiro JN, Kelm S, Baum LG, Krauss S, et al. (1998) Molecular
basis for the generation in pigs of influenza A viruses with pandemic
potential. J Virol 72: 7367-7373.
Open Access
27. Shinya K, Ebina M, Yamada S, Ono M, Kasai N, et al. (2006) Avian flu:
influenza virus receptors in the human airway. Nature 440: 435-436.
28. Bertram S, Glowacka I, Steffen I, Kühl A, Pöhlmann S (2010) Novel
insights into proteolytic cleavage of influenza virus hemagglutinin. Rev
Med Virol 20: 298-310.
29. Lai S, Qin Y, Cowling BJ, Ren X, Wardrop NA, et al (2016) Global
epidemiology of avian influenza A H5N1 virus infection in humans,
1997–2015: a systematic review of individual case data. Lancet Infect
Dis 16: e108-118.
30. Matrosovich MN, Krauss S, Webster RG (2001) H9N2 influenza A
viruses from poultry in Asia have human virus-like receptor specificity.
Virology 281: 156-162.
31. Koopmans M, Wilbrink B, Conyn M, Natrop G, van der Nat H, et
al. (2004) Transmission of H7N7 avian influenza A virus to human
beings during a large outbreak in commercial poultry farms in the
Netherlands. Lancet 363: 587-593.
32. Chen Y, Liang W, Yang S, Wu N, Gao H, et al. (2013) Human
infections with the emerging avian influenza A H7N9 virus from wet
market poultry: clinical analysis and characterisation of viral genome.
Lancet 381: 1916-1925.
33. Harder TC, Buda S, Hengel H, Beer M, Mettenleiter TC (2016) Poultry
food products—a source of avian influenza virus transmission to
humans?. Clin Microbiol Inf 22: 141-146.
34. Taubenberger JK, Morens DM (2006) 1918 Influenza: the mother of all
pandemics. Emerg Infect Dis 12: 15-22.
Citation: Murtada M, Barbour E, Shaib H (2016) Avian Influenza Infections in Humans and Poultry of Lebanon: A Mini Review. J Emerg Dis Virol 3(1): doi
http://dx.doi.org/10.16966/2473-1846.125
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